Involvement of a Stat3 binding site in inflammation-induced enteric apelin expression

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 295, Issue 5, 2008, Pages

  Han, Song ^a   Wang, Guiyun ^a   Qi, Xiang ^a   Englander, Ella W ^a   Greeley Jr , George H ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

Author keywords

Gastrointestinal tract; Lipopolysaccharide; Rodent

Indexed keywords

APELIN; GAMMA INTERFERON; INTERLEUKIN 6; INTERLEUKIN 6 ANTIBODY; JANUS KINASE; LIPOPOLYSACCHARIDE; STAT PROTEIN; STAT3 PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING SITE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; ENTERITIS; INTESTINE CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; RAT;

ANIMALS; CARRIER PROTEINS; CELLS, CULTURED; GENE EXPRESSION REGULATION; ILEUM; INFLAMMATION; INTERFERON-GAMMA; INTERLEUKIN-6; JANUS KINASES; LIPOPOLYSACCHARIDES; MICE; MICE, INBRED C57BL; MICE, NUDE; PROTEIN BINDING; RATS; RATS, SPRAGUE-DAWLEY; STAT3 TRANSCRIPTION FACTOR; STOMACH;

EID: 57349195114     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.90493.2008     Document Type: Article

References (47)

1. Atreya R, Mudter J, Finotto S, Mullberg J, Jostock T, Wirtz S, Schutz M, Bartsch B, Holtmann M, Becker C, Strand D, Czaja J, Schlaak JF, Lehr HA, Autschbach F, Schurmann G, Nishimoto N, Yoshizaki K, Ito H, Kishimoto T, Galle PR, Rose-John S, Neurath MF. Blockade of interleukin 6 trans signaling suppresses T-cell resistance against apoptosis in chronic intestinal inflammation: evidence in crohn disease and experimental colitis in vivo. Nat Med 6: 583-588, 2000.
2. Brown SJ, Mayer L. The immune response in inflammatory bowel disease. Am J Gastroenterol 102: 2058-2069, 2007.
3. Cayabyab M, Hinuma S, Farzan M, Choe H, Fukusumi S, Kitada C, Nishizawa N, Hosoya M, Nishimura O, Messele T, Pollakis G, Goudsmit J, Fujino M, Sodroski J. Apelin, the natural ligand of the orphan seven-transmembrane receptor APJ, inhibits human immunodeficiency virus type 1 entry. J Virol 74: 11972-11976, 2000.
4. Chan AS, Yip EC, Yung LY, Pang H, Luk SC, Pang SF, Wong YH. CKBM stimulates MAPKs but inhibits LPS-induced IFN-gamma in lymphocytes. Phytother Res 20: 725-731, 2006.
5. Chang CH, Chey WY, Sun Q, Leiter A, Chang TM. Characterization of the release of cholecystokinin from a murine neuroendocrine tumor cell line, STC-1. Biochim Biophys Acta 1221: 339-347, 1994.
6. Dai T, Ramirez-Correa G, Gao WD. Apelin increases contractility in failing cardiac muscle. Eur J Pharmacol 553: 222-228, 2006.
7. Daviaud D, Boucher J, Gesta S, Dray C, Guigne C, Quilliot D, Ayav A, Ziegler O, Carpene C, Saulnier-Blache JS, Valet P, Castan-Laurell I. TNFα up-regulates apelin expression in human and mouse adipose tissue. FASEB J 20: 1528-1530, 2006.
8. Edinger AL, Hoffman TL, Sharron M, Lee B, Yi Y, Choe W, Kolson DL, Mitrovic B, Zhou Y, Faulds D, Collman RG, Hesselgesser J, Horuk R, Doms RW. An orphan seven-transmembrane domain receptor expressed widely in the brain functions as a coreceptor for human immunodeficiency virus type 1 and simian immunodeficiency virus. J Virol 72: 7934-7940, 1998.
9. Farkasfalvi K, Stagg MA, Coppen SR, Siedlecka U, Lee J, Soppa GK, Marczin N, Szokodi I, Yacoub MH, Terracciano CM. Direct effects of apelin on cardiomyocyte contractility and electrophysiology. Biochem Biophys Res Commun 357: 889-895, 2007.
10. Gomez G, Zhang T, Rajaraman S, Thakore KN, Yanaihara N, Townsend CM Jr, Thompson JC, Greeley GH. Intestinal peptide YY: ontogeny of gene expression in rat bowel and trophic actions on rat and mouse bowel. Am J Physiol Gastrointest Liver Physiol 268: G71-G81, 1995.
11. Habara T, Nakatsuka M, Konishi H, Asagiri K, Noguchi S, Kudo T. The biological effects of antiadhesion agents on activated RAW264.7 macrophages. J Biomed Mater Res 61: 628-633, 2002.
12. Habata Y, Fujii R, Hosoya M, Fukusumi S, Kawamata Y, Hinuma S, Kitada C, Nishizawa N, Murosaki S, Kurokawa T, Onda H, Tatemoto K, Fujino M. Apelin, the natural ligand of the orphan receptor APJ, is abundantly secreted in the colostrum. Biochim Biophys Acta 1452: 25-35, 1999.
13. Han S, Wang G, Qi X, Lee HM, Englander EW, Greeley GH Jr. A possible role for hypoxia-induced apelin expression in enteric cell proliferation. Am J Physiol Regul Integr Comp Physiol 294: R1832-R1839, 2008.
14. Han S, Wang G, Qiu S, de la Motte C, Wang HQ, Gomez G, Englander EW, Greeley GH Jr. Increased colonic apelin production in rodents with experimental colitis and in humans with IBD. Regul Pept 142: 131-137, 2007.
15. Hirohashi N, Morrison DC. Low-dose lipopolysaccharide (LPS) pretreatment of mouse macrophages modulates LPS-dependent interleukin-6 production in vitro. Infect Immun 64: 1011-1015, 1996.
16. Hosoya M, Kawamata Y, Fukusumi S, Fujii R, Habata Y, Hinuma S, Kitada C, Honda S, Kurokawa T, Onda H, Nishimura O, Fujino M. Molecular and functional characteristics of APJ. Tissue distribution of mRNA and interaction with the endogenous ligand apelin. J Biol Chem 275: 21061-21067, 2000.
17. Ito H, Takazoe M, Fukuda Y, Hibi T, Kusugami K, Andoh A, Matsumoto T, Yamamura T, Azuma J, Nishimoto N, Yoshizaki K, Shimoyama T, Kishimoto T. A pilot randomized trial of a human anti-interleukin-6 receptor monoclonal antibody in active Crohn's disease. Gastroenterology 126: 989-996, 2004.
18. Kawamata Y, Habata Y, Fukusumi S, Hosoya M, Fujii R, Hinuma S, Nishizawa N, Kitada C, Onda H, Nishimura O, Fujino M. Molecular properties of apelin: tissue distribution and receptor binding. Biochim Biophys Acta 1538: 162-171, 2001.
19. Kunduzova O, Alet N, Delesque-Touchard N, Millet L, Castan-Laurell I, Muller C, Dray C, Schaeffer P, Herault JP, Savi P, Bono F, Valet P. Apelin/APJ signaling system: a potential link between adipose tissue and endothelial angiogenic processes. FASEB J, 2008 Aug 15 [Epub ahead of print].
20. Lago F, Dieguez C, Gomez-Reino J, Gualillo O. The emerging role of adipokines as mediators of inflammation and immune responses. Cytokine Growth Factor Rev 18: 313-325, 2007.
21. Lambrecht NW, Yakubov I, Zer C, Sachs G. Transcriptomes of purified gastric ECL and parietal cells: identification of a novel pathway regulating acid secretion. Physiol Genomics 25: 153-165, 2006.
22. Lee DK, Cheng R, Nguyen T, Fan T, Kariyawasam AP, Liu Y, Osmond DH, George SR, O'Dowd BF. Characterization of apelin, the ligand for the APJ receptor. J Neurochem 74: 34-41, 2000.
23. Liu YW, Chen CC, Tseng HP, Chang WC. Lipopolysaccharide-induced transcriptional activation of interleukin-10 is mediated by MAPK- and NF-kappaB-induced CCAAT/enhancer-binding protein delta in mouse macrophages. Cell Signal 18: 1492-1500, 2006.
24. Matsuura M, Saito S, Hirai Y, Okamura H. A pathway through interferon-gamma is the main pathway for induction of nitric oxide upon stimulation with bacterial lipopolysaccharide in mouse peritoneal cells. Eur J Biochem 270: 4016-4025, 2003.
25. Medhurst AD, Jennings CA, Robbins MJ, Davis RP, Ellis C, Winborn KY, Lawrie KW, Hervieu G, Riley G, Bolaky JE, Herrity NC, Murdock P, Darker JG. Pharmacological and immunohistochemical characterization of the APJ receptor and its endogenous ligand apelin. J Neurochem 84: 1162-1172, 2003.
26. Mitsuyama K, Matsumoto S, Rose-John S, Suzuki A, Hara T, Tomiyasu N, Handa K, Tsuruta O, Funabashi H, Scheller J, Toyonaga A, Sata M. STAT3 activation via interleukin 6 trans-signalling contributes to ileitis in SAMP1/Yit mice. Gut 55: 1263-1269, 2006.
27. Mudter J, Neurath MF. Il-6 signaling in inflammatory bowel disease: pathophysiological role and clinical relevance. Inflamm Bowel Dis 13: 1016-1023, 2007.
28. Murakami K, Bujo H, Unoki H, Saito Y. Effect of PPARalpha activation of macrophages on the secretion of inflammatory cytokines in cultured adipocytes. Eur J Pharmacol 561: 206-213, 2007.
29. O'Carroll AM, Selby TL, Palkovits M, Lolait SJ. Distribution of mRNA encoding B78/apj, the rat homologue of the human APJ receptor, and its endogenous ligand apelin in brain and peripheral tissues. Biochim Biophys Acta 1492: 72-80, 2000.
30. Pizarro TT, De La Rue SA, Cominelli F. Role of interleukin 6 in a murine model of Crohn's ileitis: are cytokine/anticytokine strategies the future for IBD therapies? Gut 55: 1226-1227, 2006.
31. Ramana KV, Fadl AA, Tammali R, Reddy AB, Chopra AK, Srivastava SK. Aldose reductase mediates the lipopolysaccharide-induced release of inflammatory mediators in RAW264.7 murine macrophages. J Biol Chem 281: 33019-33029, 2006.
32. Reaux-Le Goazigo A, Alvear-Perez R, Zizzari P, Epelbaum J, Bluet-Pajot MT, Llorens-Cortes C. Cellular localization of apelin and its receptor in the anterior pituitary: evidence for a direct stimulatory action of apelin on ACTH release. Am J Physiol Endocrinol Metab 292: E7-E15, 2007.
33. Schwarz NT, Engel B, Eskandari MK, Kalff JC, Grandis JR, Bauer AJ. Lipopolysaccharide preconditioning and cross-tolerance: the induction of protective mechanisms for rat intestinal ileus. Gastroenterology 123: 586-598, 2002.
34. Sempere L, Martinez J, de Madaria E, Lozano B, Sanchez-Paya J, Jover R, Perez-Mateo M. Obesity and fat distribution imply a greater systemic inflammatory response and a worse prognosis in acute pancreatitis. Pancreatology 8: 257-264, 2008.
35. Sorhede Winzell M, Magnusson C, Ahren B. The apj receptor is expressed in pancreatic islets and its ligand, apelin, inhibits insulin secretion in mice. Regul Pept 131: 12-17, 2005.
36. Susaki E, Wang G, Cao G, Wang HQ, Englander EW, Greeley GH Jr. Apelin cells in the rat stomach. Regul Pept 129: 37-41, 2005.
37. Suzuki A, Hanada T, Mitsuyama K, Yoshida T, Kamizono S, Hoshino T, Kubo M, Yamashita A, Okabe M, Takeda K, Akira S, Matsumoto S, Toyonaga A, Sata M, Yoshimura A. CIS3/SOCS3/SSI3 plays a negative regulatory role in STAT3 activation and intestinal inflammation. J Exp Med 193: 471-481, 2001.
38. Suzuki M, Hisamatsu T, Podolsky DK. Gamma interferon augments the intracellular pathway for lipopolysaccharide (LPS) recognition in human intestinal epithelial cells through coordinated up-regulation of LPS uptake and expression of the intracellular Toll-like receptor 4-MD-2 complex. Infect Immun 71: 3503-3511, 2003.
39. Taheri S, Murphy K, Cohen M, Sujkovic E, Kennedy A, Dhillo W, Dakin C, Sajedi A, Ghatei M, Bloom S. The effects of centrally administered apelin-13 on food intake, water intake and pituitary hormone release in rats. Biochem Biophys Res Commun 291: 1208-1212, 2002.
40. Takasuka N, Tokunaga T, Akagawa KS. Preexposure of macrophages to low doses of lipopolysaccharide inhibits the expression of tumor necrosis factor-alpha mRNA but not of IL-1 beta mRNA. J Immunol 146: 3824-3830, 1991.
41. Tatemoto K, Hosoya M, Habata Y, Fujii R, Kakegawa T, Zou MX, Kawamata Y, Fukusumi S, Hinuma S, Kitada C, Kurokawa T, Onda H, Fujino M. Isolation and characterization of a novel endogenous peptide ligand for the human APJ receptor. Biochem Biophys Res Commun 251: 471-476, 1998.
42. Tatemoto K, Takayama K, Zou MX, Kumaki I, Zhang W, Kumano K, Fujimiya M. The novel peptide apelin lowers blood pressure via a nitric oxide-dependent mechanism. Regul Pept 99: 87-92, 2001.
43. Wang G, Anini Y, Wei W, Qi X, O'Carroll AM, Mochizuki T, Wang HQ, Hellmich MR, Englander EW, Greeley GH Jr. Apelin, a new enteric peptide: localization in the gastrointestinal tract, ontogeny, and stimulation of gastric cell proliferation and of cholecystokinin secretion. Endocrinology 145: 1342-1348, 2004.
44. Wang G, Kundu RK, Han S, Qi X, Englander EW, Quertermous T, Greeley GH. Regulation of colonic trefoil factor 3 by apelin. Gastroenterology 134: A392, 2008.
45. Wang G, Qi X, Wei W, Englander EW, Greeley GH Jr. Characterization of the 5′-regulatory regions of the rat and human apelin genes and regulation of breast apelin by USF. FASEB J 20: 2639-2641, 2006.
46. Yamamoto M, Yoshizaki K, Kishimoto T, Ito H. IL-6 is required for the development of Th1 cell-mediated murine colitis. J Immunol 164: 4878-4882, 2000.
47. Ziccardi P, Nappo F, Giugliano G, Esposito K, Marfella R, Cioffi M, D'Andrea F, Molinari AM, Giugliano D. Reduction of inflammatory cytokine concentrations and improvement of endothelial functions in obese women after weight loss over one year. Circulation 105: 804-809, 2002.